Abstract
We studied the species richness of flower-visiting Hymenoptera assemblages in two varieties of Brassica campestris var. toria: in variety TS-36 during the normal season grown in the riparian ecosystem and in variety TS-67 during the late season grown in the rice-ecosystem of Assam, India using five sampling methods. We aimed to investigate to what extent (i) the Hymenoptera assemblages in the two ecosystems differed from each other, (ii) the population densities of three dominant Apis spp. differed from each other, and (iii) the effectiveness of the sampling methods used differed from each other. In total, we recorded 64 Hymenoptera species belonging to 42 genera of 9 families in the two toria varieties. We detected the presence of all species in TS-36 grown as normal season crop in the riparian ecosystem, and the presence of 48 species in TS-67 grown in the rice ecosystem as a late season crop. Vespidae had the highest species richness, followed by Apidae, Megachilidae, and Halictidae. These visitors may contribute to the ecological resilience of the toria ecosystem through their service as pollinators as well as because they are natural enemies of the crop-pests. Transect walk methods sampled a higher number of species than observation plot method and colour traps. Apis cerana was the most abundant species, with a relative abundance of 38.5% and 37.9% in normal and late season crops, respectively. The mean abundance of all three Apis species was 11.1% higher in the later variety.
Introduction
Brassica campestris L. is nearly self-sterile and yields more seeds when cross pollination occurs (William 1978). B. campestris var. toria is an insect-attractive crop with ample pollen and nectar, so it is predominantly insect-pollinated (Stanley et al. 2017). It is widely cultivated in the Northeastern Region (NER) of India (Fig. 1). The state of Assam within the NER overlaps with two global biodiversity hotspots, the Indo-Burman and the Himalayan (Myers et al. 2000). Despite having such a rich biodiversity, NER is one of the least investigated regions on the globe because of its remoteness, hilly terrain, low connectivity, and few research institutes relative to the size of the geographical area.
A map of India showing Assam in red (A) and the state of Assam enlarged showing Dibrugarh district in red (B), where the study was conducted. (Source: www.commons.wikimedia.org)
Citation: Animal Taxonomy and Ecology 70, 3; 10.1556/1777.2024.11471
Ecological intensification requires careful understanding and quantification of the beneficial ecological processes (Garbach et al. 2017), such as biological pest regulation, nutrient cycling, and insect pollination. Knowing insect diversity is important because insects play important roles in these processes. However, there is virtually no information available on the strength of pollination services and the identity of pollination service providers from Asian smallholder farming systems, where fields are small and variation among fields is high (Zou et al. 2017).
The sampling method has to be chosen very carefully to maximize efficiency and repeatability and to obtain results that best represent the ecological assemblages under study (Popic et al. 2013). The most frequently deployed method of sampling insects is the use of coloured pan traps (bowl) filled with soapy water (Leong & Thorpe 1999, Cane et al. 2000, Toller et al. 2005), accompanied by netting on nearby vegetation (Roulston et al. 2007). This is also true for investigations which have been done in NER India, where the variable transect (VT) method has never been applied for sampling flower visitors of toria crop. Even though the application of pan traps in combination with netting delivers good results, our hypothesis is that the incorporation of the VT method would further enhance the number of species collected.
We conducted an investigation on species richness of flower-visiting insects using five sampling techniques in the crop Brassica campestris var. toria grown in two ecosystems in Assam, India. We aimed to test whether (i) the Hymenoptera assemblages on the varieties TS-36 and TS-67 differ from each other, and (ii) the population of the three dominant Apis spp. differ from one another to the same extent in two varieties.
Material and methods
Study area, crop season and varieties
The study was conducted at farmers' fields of three villages viz., Jajimukh (GPS: N27° 16′ 723″; E94° 49′ 901″), Lejai Panimirigaon (GPS: N27° 17′ 06.9″; E94° 48′ 08.5″), and Bhagamur (GPS: N27° 16′ 826″; E94° 49′ 967″) in Dibrugarh district of Assam state, India. The villages are situated near the river Burhidihing, one of the district's major toria production areas. In each village, two crops of toria are grown per year in two sites: variety TS-36 in the normal season near the river and TS-67 in the late season in the rice field. We collected data during four sampling periods: one during the normal and one during the late season in 2015–16, which we repeated in 2016–17 in the same sites. The samplings were repeated in the same fields for the respective crop. In each of the above mentioned sites, the data were taken weekly for eight weeks during the sampling periods. Variety TS-36 was sown in mid-October (i.e., the normal season) and sampling of insect-visitors was done from mid-November to mid-January, whereas TS-67 was sown in the 2nd week of December (i.e., the late season) and sampling of insect-visitors was done from mid-January to mid-February. The eight weeks of sampling covered crop stages with five different flowering densities with a variable number of flowers per square meter i.e. (i) Low: 25–123/m2, (ii) Medium: 217–381/m2, (iii) High: 487–742/m2, (iv) Medium back: 168–387/m2, and (v) Low back: 23–107/m2.
Normal season crop (normal crop hereafter) was sown in the riparian ecosystem which was characterised by the presence of toria as the main crop on hundreds of hectares in medium and upland situations, with other winter crops (pulses, spinach, potato, onion, garlic etc.) cultivated in between toria fields and the river. The surrounding vegetation was diverse in non-cropped areas, consisting of a wide variety of tree, shrub, and herb species, as well as bamboo stands.
Late season toria crop (late crop hereafter) was sown in the rice ecosystem in medium-low lands after the harvest of mid-duration rice crop on less than half the acreage of the normal crop. Toria fields were surrounded by rice-fallow lands or homestead gardens in the typical Baari system or by a river bank on one side. The Baari system is a homestead garden characterised by the presence of rich floral diversity with a variety of trees, shrubs, herbs, medicinal plants and bamboo plantations, mostly on the rear side of villagers' gardens.
Sampling methods of flower visitors
Five sampling methods were used in order to record the species richness of Hymenopteran visitors. The methodology and sampling design was as described by Westphal et al. (2008), Nielsen et al. (2011), and Belavadi and Ganeshaiah (2013).
Observation plots (OP) method: In each study site, ten rectangular observation plots of 1 × 2 m each were established in random locations. Observations at each plot lasted for 6 min in each occassion. During the observation period, every Hymenopteran specimen was collected for identification.
Standardised transect walks (ST) method: We permanently marked a 250 m long and 4 m wide corridor (transect) and divided it into 10 subunits. Each subunit was surveyed for 5 min during which all the hymenopterans visiting the toria flowers were collected by netting.
Variable transect walks (VT) method: To cover better the spatially heterogeneous distribution of floral resources, thereby increasing the probability of finding a higher proportion of the Hymenoptera species present, an additional 1 ha plot was set out for VT sampling adjacent to the area where the other sampling methods were applied. In the VT plots we slowly walked around for 30 min and captured hymenopterans by netting.
Sampling in OP, ST and VT was conducted between 8:00 AM and 4:00 PM. The sequence of the observations in different fields was randomised to occur at different hours of the day and thereby avoid temporal bias.
Elevated bowl traps (EBT) method: In each study site, 30 bowl traps were set up in 10 clusters separated by 15 m. Each cluster contained bowl traps in three colours (white, yellow, and blue) to account for different colour preferences of bee species, thereby increasing the trap clusters' efficiency in attracting bees (Leong & Thorpe 1999, Toler et al. 2005). Each trap was filled with 200 ml of water and a few drops of liquid detergent. The traps were mounted on a pole at canopy height and left active for 48 h during each of the eight rounds of sampling.
Ground bowl trap (GBT) method: In each study site, we placed 30 coloured bee-bowls in 10 clusters of three colours (yellow, white, and blue) on the ground at 15 m intervals. We used both ground-level and canopy-level traps to catch both the epigean and arboreal visitors.
The collected specimens were dried in the shade, segregated, and stored in alcohol for future identification. Taxonomic identification of the collected specimens was done at the ICAR-National Bureau of Agricultural Insect Resources, Bengaluru, and at the University of Agricultural Sciences, Bengaluru, India. In some instances, we referred to the Global Biodiversity Identification Facility database (https://www.gbif.org).
Statistical analyses
The abundance data were analysed using the software SPSS version 20. ANOVA was used to compare the mean difference in treatments with the “Tukey” post-hoc method.
Results
We recorded a total of 64 hymenopteran species (Table 1). All species were recorded in the normal crop, whereas 48 species were recorded in the late crop (Table 2). The 16 species only found in the normal crop were 4 species of Apidae, 4 of Vespidae, 3 of Halictidae, 2 of Crabronidae, 2 of Specidae and 1 of Scolidae. Vespidae was present with the highest species richness, with 11 genera and 18 species, followed by Apidae (7 genera and 15 species) in the normal season crop (Table 2). Megachilidae, Halictidae and Colletidae were the families with the lowest species richness. Out of the 42 genera recorded, 7 genera viz., Apis, Ceratina, Amegellia, Megachile, Polistes, Delta and Lasioglossum were represented by 3 species each, while the other genera by two or just one species (Table 1).
Summary of Hymenopteran species observed in Brassica campestris var. toria in Assam, India
| No. | Family | Name of genus (No. of species) | No. of genus, species, relative richness (%) | |||
| Genus | % | Species | % | |||
| 1 | Apidae | Apis (3); Ceratina (3); Xylocopa (2); Tetragonula (1); Amegellia (3); Thyreus (2); Anthophora (1). | 7 | 16.7 | 15 | 23.4 |
| 2 | Andrenidae | Andrena (2). | 1 | 2.4 | 2 | 3.1 |
| 3 | Megachilidae | Megachile (3); Anthidium (1); Coelioxys (1); Anthidiellum (1); Lithurgus (1); Chelostoma (1). | 6 | 14.3 | 8 | 12.5 |
| 4 | Vespidae | Vespa (2); Ropalidia (1); Polistes (3); Parapolybia (1); Rhynchium (2); Antodynerus (1); Delta (3); Phimenes (1); Allorhynchium (1); Zethus (1); Subancistrocerus (2). | 11 | 26.2 | 18 | 28.1 |
| 5 | Scoliidae | Scolia (1); Unknown genus other than Scolia (1) | 2 | 4.8 | 2 | 3.1 |
| 6 | Halictidae | Nomia (1); Hoplonomia (1); Curvinomia (1); Halictus (2); Sphecodes (1); Lasioglossum (3). | 6 | 14.3 | 9 | 14.1 |
| 7 | Crabronidae | Bemix (1); Cerceris (2); Tachysphex (1); Larra (1). | 4 | 9.5 | 5 | 7.8 |
| 8 | Colletidae | Colletes (1) | 1 | 2.4 | 1 | 1.6 |
| 9 | Sphecidae | Chalybion (1); Sceliphron (1); Chlorion (1); Sphex (1). | 4 | 9.5 | 4 | 6.3 |
| Total: 9 families; 42 genera; 64 species | 42 | 100% | 64 | 100% | ||
Hymenopteran flower-visitors in the normal crop (variety TS-36) and the late crop (variety TS-67). The sampling methods used were observation plot (OP), standardized transect walk (ST), variable transect walk (VT), elevated bowl trap (EBT) and ground bowl trap (GBT). The ‘+’ and ‘−’ signs in the table indicate the species found or not found in the respective ecosystem
| Sl No. | Species | Sampling method effective in capturing specimens | Ecosystem & variety | |
| Riparian (TS-36) | Rice (TS-67) | |||
| Family: Apidae | ||||
| 1 | Apis cerana Fabricius, 1793 | All methods | + | + |
| 2 | Apis florae Fabricius, 1787 | All methods | + | + |
| 3 | Apis dorsata Fabricius, 1793 | EYT, EWT, OP, ST, VT | + | + |
| 4 | Ceratina binghami Cockerell, 1908 | EYT, GYT, GWT, OP, ST, VT | + | + |
| 5 | Ceratina perforatrix Smith, 1879 | EYT, EBT, GYT, ST, VT | + | + |
| 6 | Ceratina sp. | VT | + | – |
| 7 | Xylocopa fenestrata (Fabricius, 1798) | OP, ST, VT | + | + |
| 8 | Xylocopa aestuans (Linnaeus, 1758) | OP, ST, VT | + | + |
| 9 | Tetragonula iridipennis (Smith, 1854) | EYT, GYT, GWT, GBT, ST, VT | + | + |
| 10 | Anthophora sp. | VT | + | – |
| 11 | Amegillia zonata (Linnaeus, 1758) | EYT, OP, ST, VT | + | + |
| 12 | Amegillia cingulata (Fabricius, 1775) | VT | + | + |
| 13 | Amegillia sp | VT | + | – |
| 14 | Thyreus sp. | EYT, ST. | + | – |
| 15 | Thyreus ramosus (Lepeletier, 1841) | EWT, VT | + | + |
| Family: Vespidae | ||||
| 1 | Vespa cincta Fabricius, 1775 | OP, ST, VT | + | + |
| 2 | Vespa tropica (Linnaeus, 1758) | ST, VT | + | + |
| 3 | Ropalidia marginata (Lepeletier, 1836) | VT | + | + |
| 4 | Parapolybia indica (de Saussure, 1854) | ST, VT | + | + |
| 5 | Polistes hebraeus Fabricius, 1787 | ST, VT | + | + |
| 6 | Polistes tenebricosus Lepeletier, 1863 | YET | + | + |
| 7 | Polistes olivaceus (Deg., 1773) | EYT, ST, VT | + | + |
| 8 | Rhynchium brunneum (Fabricius, 1793) | VT | + | + |
| 9 | Rhynchium carnaticum (Fabricius, 1798) | VT | + | – |
| 10 | Antodynerus limbatus (de Saussure, 1852) | VT | + | – |
| 11 | Delta conoideum (Gmelin, 1790) | OP, ST, VT | + | + |
| 12 | Delta esuriens (Fabricius, 1787) | VT | + | + |
| 13 | Delta pyriforme (Fabricius, 1775) | VT | + | + |
| 14 | Phimenes flavopictus (Blanchard, 1845) | EYT, OP, ST, VT | + | + |
| 15 | Zethus sp. | VT | + | – |
| 16 | Allorhynchium argentatum (Fabricius, 1804) | ST | + | – |
| 17 | Subancistrocerus sichelii (de Saussure, 1856) | VT | + | + |
| 18 | Subancistrocerus camicrus (Cameron, 1904) | VT | + | + |
| Family: Halictidae | ||||
| 1 | Nomia sp. | EYT, GYT, GBT, ST, VT. | + | + |
| 2 | Hoplonomia sp | EYT, GYT, GWT, ST. | + | + |
| 3 | Curvinomia iridescens (Smith, 1853) | VT. | + | – |
| 4 | Halictus sp. | EYT, ST, VT. | + | + |
| 5 | Halictus scabiosae (Rossi, 1790) | EYT, EWT, EBT, ST, VT | + | + |
| 6 | Sphecodes sp. | VT | + | – |
| 7 | Lasioglossum sp.1 | GYT, GBT, EYT, ST, VT | + | + |
| 8 | Lasioglossum sp.2 | GYT, GBT, GWT, EYT, ST, OP | + | + |
| 9 | Lasioglossum sp 3 | GYT, VT | + | – |
| Family: Crabronidae | ||||
| 1 | Bemix sp | ST, VT | + | + |
| 2 | Cerceris sp.1 | GYT, GWT, ST, VT | + | + |
| 3 | Cerceris sp.2 | EYT, EBT, ST | + | + |
| 4 | Tachysphex sp. | VT | + | – |
| 5 | Larra sp. | VT | + | – |
| Family: Megachilidae | ||||
| 1 | Megachile laticeps Smith, 1853 | EYT, OP, ST, VT | + | + |
| 2 | Megachile lanata (Fabricius, 1775) | OP, EWT, ST | + | + |
| 3 | Megachile carbonaria Smith, 1853 | VT | + | + |
| 4 | Anthidium sp | GYT, VT | + | + |
| 5 | Coelioxys sp | EYT, OP, ST, VT. | + | + |
| 6 | Lithurgus sp. | ST, VT | + | + |
| 7 | Chelostoma sp | EYT, VT | + | + |
| 8 | Anthidiellum sp. | EYT, ST. | + | + |
| Family: Sphecidae | ||||
| 1 | Chalybion bengalense (Dahlbom, 1845) | VT | + | + |
| 2 | Sceliphron curvatum (F.Smith, 1870) | ST, VT | + | + |
| 3 | Chlorion sp. | VT | + | – |
| 4 | Sphex argentatus Fabricius, 1787 | ST, VT. | + | – |
| Family: Andrenidae | ||||
| 1 | Andrena sp.1. | EYT, GYT, GWT, GBT, ST | + | + |
| 2 | Andrena sp.2 | OP, VT | + | + |
| Family: Scoliidae | ||||
| 1 | Scolia soror (Smith, 1855) | ST, VT | + | + |
| 2 | Unknown scoliidae1 | VT | + | – |
| Family:Colletidae | ||||
| 1 | Colletes sp | VT | + | + |
| Total no. of species observed: | 64 | 48 | ||
We found the three species of Apis in higher numbers than any other hymeopteran species in all sampling locations, irrespective of the variety grown. Apis cerana was the most abundant flower-visitor with a mean abundance of 5.71 ± 2.25 (mean ± SD) per sqm in the normal crop and 6.25 ± 2.16 per sqm in the late crop (Table 3). A. cerana was the most abundant species; however, A. cerana and A. florea were at par in the riparian ecosystem i.e. in normal crops.
Mean abundance (no./sqm) of wild Apis spp. in toria crop in two crop seasons. Numbers represent means ± SD of the corresponding data recorded in three locations over two years. Superscripted letters indicate homogeneous subsets according to post-hoc tests (P = 0.01)
| Pollinator species | Normal crop (Riparian: TS-36) | Late crop (Rice: TS-67) |
| Apis cerana | (5.71 ± 2.25)a | (6.25 ± 2.16)a |
| Apis florae | (5.57 ± 1.99)a | (5.99 ± 2.01)b |
| Apis dorsata | (3.55 ± 1.18)b | (4.23 ± 1.22)c |
Tabulated data are mean of the corresponding data recorded in three locations for two years. In the mean column, the values superscripted by a common letter(s) are at par.
Among the sampling methods (Fig. 2), VT sampled the highest number of hymenoptera species (55; 85.9%), followed by ST (56.3%), EBT (39.06%), OP (23.4%) and GBT (20.31%). Among the coloured traps, EYT sampled the highest number of species (35.9%) followed by GYT (20.3%), GWT (12.5%), GBT (10.9%), EWT (9.4%), and EBT (7.8%).
Hymenoptera species number sampled by different methods {WCT (White colour trap) includes the number of species sampled by EWT (Elevated White Trap) and GWT (Ground White Trap). BCT: (Blue colour trap) includes species sampled by EBT (Elevated Blue Trap) and GBT (Ground Blue Trap). YCT: (Yellow colour trap) includes species sampled EYT (Elevated Yellow Trap) and GYT (Ground Yellow Trap). The common species sampled by two same colour traps at ground and canopy have been considered once for counting. VT: Variable Transect; ST: Standardised transect; OP: Observation plot}
Citation: Animal Taxonomy and Ecology 70, 3; 10.1556/1777.2024.11471
Discussion
The riparian ecosystem is traditionally used for cultivating toria in Assam, whereas its cultivation in the rice ecosystem is a new venture. Therefore, the interactions between toria and its flower visitors are more stable and better established in the riparian ecosystem. With the advent of the new variety, TS-67, developed by the Assam Agricultural University, Jorhat the farmers have started growing it as a late crop in the rice ecosystem following a mid-duration rice variety to meet the increasing demand of edible oil. However, the late crop is not very popular in Assam. We may expect that with the popularisation of late varieties of toria among farmers and a consequent increase in its acreage may result in more flower visitors to toria crops grown in rice ecosystems in the future.
We recorded 64 species of Hymenopteran visitors in Brassica spp. many of which have also been reported previously from India (Kunjwal et al. 2014, Roy et al. 2014, Devi et al. 2017, Srivastava et al. 2017, Thangjam et al. 2016) and Nepal (Pudasaini & Thapa 2014, Pudasaini et al. 2015 Pudasaini et al. 2014, Rijal et al. 2017). Several species of Apis, Xylocopa, Tetragonula, Amegellia, Thyreus, Vespa, Polistes, Delta, Scolia, Phimenes, Halictus, and Sceliphron have also been reported from the adjoining states of Assam by Thakur et al. (2013).
We found difference in the abundance of three Apis bees in both the crops (Table 3). A. cerana was found to be the most abundant species with a relative abundance of 38.5% in normal crop and 37.9% in late crop. A. dorsata was the least abundant species with a relative abundance of 23.9% in normal crop and 25.7% in late crop. The relatively low abundance of A. dorsata may be attributed to its specific need for nesting in tall structures (e.g. trees, buildings etc.) (Nagar et al. 2016, Sihag 2017). Moreover, the hives of A. dorsata are more vulnerable to attacks by predatory birds as compared to that of the other two Apis species because the hives of A. dorsata are large and are built in exposed places whereas the hives of the other two species are much smaller and mostly remain hidden in bushes, cavities, inside the trunks of trees, other non-crop vegetation and even in discarded structures with suitable holes pipes. Similar nesting behaviour of Apis bees has also been reported from Thailand (Seeley et al. 1982).
The population size of all three Apis spp. was larger in the late crop; this may be due to the period of high food availability in the previous normal crop. The knowledge that these two varieties are such a good combination from the standpoint of pollination is good input for farmers growing toria.
We found many flower visitors other than Apis species as listed in the tables. Such non-Apis species, besides contributing to the pollination of crop plants, also assure the pollination of wild plant species, which in turn assure the survival of Apis species during off-seasons, when there is no crop in the field.
Andrena spp. were recorded and were found making nests gregariously at the base of bamboo plantations, more often in riparian ecosystems. Such a gregarious nesting habit of A. bellidoides has been reported from the Western Ghats of India (Batra 1977), and the preference for sandy soil by Andrena species has also been reported from diverse habitats across the continental United States (Cane 1996).
Anthophora bees were also observed emerging in the early morning from the base of bamboo plantations near the river banks. In Punjab, India, A. antiope has been reported from Beas River (Batra 1980). Michener (2007) also reported Anthophora species to be solitary and to exhibit soil nesting behaviour. In East Africa, these bees were reported from various habitats, including riparian areas (https://keys.lucidcentral.org/keys/v3/eafrinet/bee_genera/key/african_bee_genera/Media/Html_eafrica/Anthophora_bees.htm).
Nomia bees were found to leave their nests situated at the base of bamboo-plantations very early in the morning for foraging. Most species of Nomia are reported to be solitary ground-nest-dwellers, but some species also nest communally, where females share a nest with queen or worker castes (Hannan et al. 2013).
The observed species of Amegilla were faster in foraging than Apis bees i.e. number of flower visited per unit time by Amegilla was more and tended to prefer over toria flowers flowers with cone shaped corolla, such as Impatiens balsamina L., a common wild weed species of Assam. Conservation of such plant species should be encouraged in non-cropped areas in toria ecosystems to bring them near toria canopy and harness their pollination service. Amala and Shivalingaswamy (2017) have established that A. zonata could be a viable buzz-pollinating bee for the pollination of tomatoes. We recorded three unknown species of Lasioglossum in toria crop even if these were not as abundant as A. zonata. The occurrence of Anthidium was more confined to non-cropped areas near toria fields, where wooden logs were kept. From Egypt, Mahfouz et al. (2012) reported Anthidium as a pollinator in sesame, another popular oilseed crop of Assam.
All species of Ceratina were detected by netting during variable transect walks, whereas Standard transect and Observation plot methods detected only two species. In a similar study conducted in Australia (Roulston 2007), netting also performed better than trapping. Contradictory to our result, C. australensis was observed in the white trap but not in the yellow trap as observed by Gollan et al. (2011) in New South Wales, Australia.
Notably, we recorded Curvinomia iridescens (Smith, 1853) on toria crop for the first time in Assam. Manjusha and Jobiraj (2018) published a checklist of the Nomiinae subfamily of Kerala, which included N. iridescens.
Sphex argentatus Fabricius, 1787 was recorded while sampling by variable transects walk. Two species of Sphex in mustard and one species in Brassica napus were reported from Himachal Pradesh, India (Devi et al. 2017) and Pakistan (Akhtar et al. 2018), respectively. Its presence was mostly confined to the border of toria plots and to the non-crop vegetation of riparian plant communities. No individual of this species was observed in the middle plots of the toria fields. There is a need to study the edge effect and weed diversity in the non-crop vegetation of the toria ecosystem for better understanding the relation between wild pollinators and weed flora.
Coelioxys spp. was observed for the first time in toria in Assam. It was earlier reported from another district (Jorhat) of the state by Rajkumari et al. (2014), but not from a toria ecosystem. Coelioxys has also been reported as a pollinator in vegetables and oilseeds in Egypt (Hussein & Abdel-Aal 1982).
An unknown species of Lithurgus was also observed in toria in a previous report from other crop-ecosystems of Jorhat, Assam (Rajkumari et al. 2014) and also from Kaziranga and Dibrugarh, Assam (www.geocities.com/BeesIndia2). Likewise, Polistes wasps were recorded for the first time from a toria ecosystem of Assam but were reported earlier by Kumar (2010) from other ecosystems. It is observed that all the three Polistes species were more abundant in peripheral vegetations especially where Glycosmis pentaphylla (Retz) DC plant was common. However, a preference of these hymenopterans to toria and to G. pentaphylla remains to be proven.
Parapolybia was observed for the first time in toria crop in Assam. This species was also observed at high abundance on Ziziphus plants near the toria fields. Parabolia have also been reported from other Asian countries (Saito-Morooka et al. 2015).
Scolia soror (Smith, 1855) is recorded for the first time in toria ecosystem of Assam; however, two species of scoliid wasps viz., Triscolia ardens (Smith, 1855) and Scolia soror (Smith, 1855) have been reported from Meghalaya, an adjoining state of Assam by Thakur et al. (2013).
More extensive studies on wild pollinator species are needed in relation to their identification, roles in pollination, conservation and augmentation to develop effective strategies for harnessing their pollination services at a maximum by small-holding farmers of Assam. Zou et al. (2017) reported an enhancement of yield in oilseed rape due to pollination by wild bees in the smallholder farming system in China.
Among the sampling methods (Fig. 2), the two transect methods (VT & ST) sampled a higher number of hymenoptera species as compared to the non-transect methods. This was most probably due to the larger size of the sampled area. The area sampled is 1,000 sqm under ST and 1 ha in VT, which are much larger than in case of the other methods and this seems not to be offset by the time factor (i.e., traps were present for 384 h while nettings along transects were performed only for 6.67 h in ST and 4 h in for VT on entire 8 occasions of sampling; similarly in Obseravation Plots the sampling was performed for 8 h altogether). The sampling efficiency, measured by number of species sampled per unit time, of the different methods are - 0.03/hr in GBT, 0.07/hr in EBT, 1.88/hr in OP, 5.40/hr in ST and 13.75/hr in VT. Moreover, there is little difference in monetary expenditure (i.e. cost of material & labour) among the sampling methods which will not affect the above cited rank of sampling efficiency even we calculate it in terms of number of species sampled per unit expenditure (say, number of species sampled/1,000 Rupees). Every method is unique; however, VT and EBT can be the best duo provided one must pay equal attention to both arboreal and epigean species during VT in order to exclude GBT.
The late crop in rice-fields is not very popular in Assam, primarily because of the large-scale cultivation of longer-duration rice varieties and the damage stray cattle can do after rice was harvested. Therefore, the cultivation of medium duration varieties of rice followed by late season toria cultivation will not only assure sufficient oil production but also increase the cropping intensity and productivity of the same piece of land. Keeping away stray cattle is possible in rice-fields (rice-toria-rice sequence) by using solar-cum-electric fencing in the crop ecosystem of Assam (Sarma et al. 2021). The community approach, where participation of all the farmers sharing a common rice-field, will bring a greater success in minimizing damage done by stray cattle and boost the socio-economic condition of poor farmers.
The present multisampling study is the first of its kind in the state of Assam. We have used transact walk, observation plot and colour traps at both ground and canopy level. No previous study used all these sampling methods together in sampling study. It is expected that the information generated from this study will form a benchmark for similar studies. It would be interesting to see the change in Hymenopteran assemblage, if any, under changing climate in the future.
Funding
No funding received for the work.
Acknowledgement
The authors acknowledge the help of scientists of the ICAR-NBAIR and UAS, Bengaluru, India for the taxonomic identification of the insect species. The authors are also grateful to the farmers of research locations for sharing their crop fields for the study and the logistic support provided for the night stay in the village during the investigation.
References
Akhtar T, Aziz MA, Naeem M, Ahmed MS, Bodlah I (2018) Diversity and relative abundance of pollinator fauna of canola (Brassica napus L. Var. Chakwal Sarson) with managed Apis mellifera L. in Pothwar Region, Gujar Khan, Pakistan. Pakistan Journal of Zoology 50(2): 567–573. https://doi.org/10.17582/journal.pjz/2018.50.2.567.573
Amala U, Shivalingaswamy TM (2017) Role of native buzz pollinator bees in enhancing fruit and seed set in tomatoes under open field conditions. Journal of Entomology and Zoological Studies 5(3): 1742–1744.
Batra SWT (1977) Bees of India (Apoidea), their behaviour, management and a key to the genera. Oriental Insects 11(3): 289–324. https://doi.org/10.1080/00305316.1977.10433811
Batra SWT (1980) Nests of the solitary bee, Anthophora antiope, in Punjab, India. Journal of the Kansas Entomological Society 53(1):112–114.
Belavadi VV, Ganeshaiah KN (2013) Insect pollination manual. Indian Council of Agricultural Research, New Delhi, India.
Cane JH (1996) Ground-nesting bees: The neglected pollinator resource for agriculture. In: Pollination – From theory to practise, 7th international symposium on pollination, Lethbridge, Canada.
Cane, JH, Minckley, RL, Kervin, RJ (2000) Sampling bees (Hymenoptera: Apiformes) for pollinator community studies: Pitfalls of pan trapping. Journal of Kanas Entomologial Society 73: 225–231.
Devi M, Sharma HK, Thakur RK, Bhardwaj SK, Rana K, Thakur M, Ram B (2017) Diversity of insect pollinators in reference to seed set of mustard (Brassica juncea L.). International Journal of Current Microbiology and Applied Sciences 6(7): 2131–2144. https://doi.org/10.20546/ijcmas.2017.607.250
Garbach K, Milder JC, Declerck FAJ, Dewit MM, Driscoll L, Gemmill-herren B (2017) Examining multi-functionality for crop yield and ecosystem services in five systems of agroecological intensification. International Journal of Agricultural Sustainability 15(1): 11–28. https://doi.org/10.1080/14735903.2016.1174810
Gollan JR, Michael BA, Michael B (2011) Comparison of yellow and white pan traps in surveys of bee fauna in New South Wales, Australia (Hymenoptera: Apoidea: Anthophila). Australian Journal of Entomology 50: 174–178. https://doi.org/10.1111/j.1440-6055.2010.00797.x
Hannan MA, Maeta Y, Miyanaga R (2013) Nesting biology and life cycle of Nomia (Acunomia) chalybeata Smith on Iriomote Island, southernmost Archipelago of Japan, with notes on the simultaneous occurrence of diapausing and non-diapausing prepupae within the same nests (Hymenoptera: Halictidae). Journal of the Saudi Society of Agricultural Sciences 12(2): 91–99. https://doi.org/10.1016/j.jssas.2012.08.002
Hussein MH, Abdel-aal SA (1982) Wild and honeybees as pollinators of 10 plant species in Assiut area, Egypt. Journal of Applied Entomology 93(1–5): 342–346. https://doi.org/10.1111/j.1439-0418.1982.tb03606.x
Kumar PG (2010) New Distributional records of some species of the subgenus Polistes (Gyrostoma) Kirby (Hymenoptera: Vespidae) from various states of India and adjacent countries. Records of Zoological Survey of India 110(4): 4–45.
Kunjwal N, Kumar Y, Khan MS (2014) Flower-visiting insect pollinators of brown mustard, Brassica juncea (L.) Czern and cross and their foraging behaviour under caged and open pollination. African Journal of Agricultural Research 9(16): 1278–1286. https://doi.org/10.5897/AJAR2013.8075
Leong JM, Thorpe RW (1999) Colour-coded sampling: The pan trap colour preferences of oligolectic and nonoligolectic bees associated with a vernal pool plant. Ecological Entomology 24: 329–335. https://doi.org/10.1046/j.1365-2311.1999.00196.x
Mahfouz HM, Kamel, SM, Belal AH, Said M (2012) Pollinators visiting sesame (Sesamum indicum L.) seed crop with reference to foraging activity of some bee species. Cercetări Agronomice în Moldova 45(2): 49–55.
Manjusha KT, Jobiraj T (2018) New record of Leuconomia brevipes from India with a checklist of Nominid bees (Apoidea: Halictidae: Nomiinae) from Kerala. Journal of Experimental Zoology 21(2): 897–900.
Michener CD. (2007) The bees of the world. John Hopkins University Press, Baltimore and London.
Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GA, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403(6772): 853–858. https://doi.org/10.1038/35002501
Nagir MT, Atmowidi T, Kahono S. (2016) The distribution and nest-site preference of Apis dorsata binghami at Maros Forest, South Sulawesi, Indonesia. Journal of Insect Biodiversity 4(23): 14.
Nielsen A, Steffan-Dewenter I, Westphal C, Messinger O, Simon, GP, Roberts SPM, Settele J, Szentgyorgyi H, Vaissiere BE, Vaitis M, Woyciechowski M, Bazos I, Beismeijer JC, Bommarco R, Kunin WE, Tscheulin T, Lamborn E, Petanidou T (2011) Assessing bee species richness in two Mediterranean communities: Importance of habitat type and sampling techniques. Ecological Research 26: 969–983. https://doi.org/10.1007/s11284-011-0852-1
Popic TJ, Davila YC, Wardle GM (2013) Evaluation of common methods for sampling invertebrate pollinator assemblages: Net sampling out-perform pan traps. Plos One 8(6): e66665. https://doi.org/10.1371/journal.pone.0066665
Pudasaini R, Thapa RB (2014) Effect of pollination on rapeseed (Brassica campestris L. var. toria) production in Chitwan, Nepal. The Journal of Agriculture and Environment 15: 41–45. https://doi.org/10.3126/aej.v15i0.19814
Pudasaini R, Thapa RB, Poudel PR (2014) Effect of pollination on qualitative characteristics of rapeseed (Brassica campestris L. var. toria) seed in Chitwan, Nepal. International Journal of Biological, Food, Veterinary and Agricultural Engineering 8(12): 1278–1281.
Pudasaini R, Thapa RB, Chaudhary NK, Tiwari S (2015) Insect pollinators’ diversity of rapeseed (Brassica campestris var. toria) in Chitwan, Nepal. Journal of the Institute of Agriculture and Animal Science 33–34: 73–78. https://doi.org/10.3126/jiaas.v33i0.20688
Rajkumari P, Sharmah D, Rahman A, Patgiri P (2014) Diversity and distribution pattern of hymenoptera insects in Jorhat District, Assam, India. International Journal of Science and Research 3(12): 1938–1941.
Rijal SP, Thapa RB, Sharma MD, Sah SK, Yubak Dhoj GC (2017) Pollinators diversity and their effects on rapeseed (Brassica campestris L. var. toria) production and productivity in Chitwan, Nepal. The Journal of Agriculture and Environment 18: 151–161. https://doi.org/10.3126/aej.v18i0.19900
Roulston TH, Smith SA, Brewster AL (2007) A comparison of pan trap and intensive net sampling techniques for documenting a bee (Hymenoptera: Apiformes) fauna. Journal of the Kansas Entomological Society 80(2): 179–181. https://doi.org/10.2317/0022-8567(2007)80[179:ACOPTA]2.0.CO;2
Roy S, Gayen AK, Mitra B, Duttagupta A (2014) Diversity, foraging activities of the insect visitors of mustard (Brassica juncea Linnaeus) and their role in pollination in West Bengal. The Journal of Zoology Studies 1(2): 7–12.
Saito-Morooka F, Nguyen LTP, Kojima J (2015) Review of the paper wasps of the Parapolybia indica species-group (Hymenoptera: Vespidae, Polistinae) in eastern parts of Asia. Zootaxa 3947(2): 215–235. https://doi.org/10.11646/zootaxa.3947.2.5
Sarma AK, Bhattacharyya HK, Barooah A, Thakuria C, Kachari M, Saikia H, Salam A (2021) A study on electric-cum-solar fencing as a tool for facilitating multiple-cropping in area with open-grazing by stray-cattle. Journal of Community Mobilization and Sustainable Development 16(3): 1036–1038. https://www.researchgate.net/publication/359203115
Seeley TD, Seeley RH, Akratakul P (1982) Colony defense strategies of the Honeybees in Thailand. Ecological Monographs 52(1): 43–63. https://doi.org/10.2307/2937344
Sihag RC (2017) Nesting behavior and nest site preferences of the giant honey bee (Apis dorsata F.) in the semi-arid environment of north west India. Journal of Apicultural Research 56(4): 452–466. https://doi.org/10.1080/00218839.2017.1338443
Srivastava K, Sharma D, Singh S, Ahmad H (2017) Foraging behaviour of honeybees in seed production of Brassica oleracea var. italica Plenck. Bangladesh Journal of Botany 46(2): 675–681.
Stanley J, Sah K and Subbanna ARNS (2017) How efficient is the Asian honeybee, Apis cerana in pollinating mustard, Brassica campestris var. toria? Pollination behavior, pollinator efficiency, pollinator requirements and impact of pollination. Journal of Apicultural Research 56(4): 439–451. https://doi.org/10.1080/00218839.2017.1329796
Thakur NSA, Rahman Z, Saikia K, Behere GT, Ngachan SV, Ramamurthy VV (2013) Insect fauna of Northeastern Himalaya. Vol. 1. Indian Council of Agricultural Research Complex for NEH Region, Umiam, Meghalaya, India.
Thangjam R, Deka MK, Borah RK, Singh HR, Buragohain P (2016) Diversity of insect pollinators and foraging behaviour of honeybee, Apis dorsata on rapeseed crop. Annals of Plant Protection Science 24(1): 83–85.
Toler TR, Evans EW, Tepedino VJ (2005) Pan-trapping for bees (Hymenoptera: Apiformes) in Utah’s West Desert: The importance of color diversity. Pan Pacific Entomologist 81(3–4): 103–113.
Westphal C, Bommarco R, Carre´ G, Lamborn E, Morison N, Petanidou T, Potts SG, Roberts SPM, Szentgyorgyi H, Tscheulin T, Vaissie`Re BE, Woyciechowski M, Biesmeijer JC, Kunin WE, Settele J, Steffan-Dewenter I (2008) Measuring bee biodiversity in different European habitats and biogeographical regions. Ecological Monographs 78(4): 653–671. https://doi.org/10.1890/07-1292.1
Williams IH (1978) The pollination requirements of swede rape (Brassica napus L.) and of turnip rape (Brassica campestris L.). The Journal of Agricultural Science 91(2): 343–348. https://doi.org/10.1017/S0021859600046438
Zou Y, Xiao H, Bianchi FJJA, Jauker F, Luo S, Werf WV (2017) Wild pollinators enhance oilseed rape yield in small-holder farming systems in China. BMC Ecology 17(6). https://doi.org/10.1186/s12898-017-0116-1
